Direct evidence for homotypic, glia-independent neuronal migration

Abstract

Neuronal precursors born in the subventricular zone (SVZ) of the neonatal and adult rodent brain migrate 3-8 mm from the walls of the lateral ventricle into the olfactory bulb. This tangentially oriented migration occurs without the guidance of radial glia or axonal processes. The cells move closely associated, forming elongated aggregates called chains, which are ensheathed by astrocytes. We have developed a culture system in which postnatal mouse SVZ neuronal precursors assemble into chains with ultrastructural and immunocytochemical characteristics equivalent to those in vivo but without the astrocytic sheath. Time-lapse videomicrography revealed that individual cells migrate along the chains very rapidly (approximately 122 microm/hr) in both directions. Periods of cell body translocation were interspersed with stationary periods. This saltatory behavior was similar to radial glia-guided migration but approximately 4 times faster. Neuronal precursors isolated from embryonic cortical ventricular zone or cerebellar external granule layer did not form chains under these conditions, suggesting that chain migration is characteristic of SVZ precursors. This study directly demonstrates that SVZ neuronal precursors migrate along each other without the assistance of astrocytes or other cell types. (Additional data are presented in www.cell.com).